Adaptive phenotypic plasticity describes the phenomenon in which a single genotype can produce a variety of phenotypes that match their environments. Like any trait, plasticity is a phenotype that can exhibit variation, but despite the ecological importance of plasticity variation, little is known about its genetic basis. Here we use the pea aphid to investigate the genetic basis of wing plasticity variation. Previous reports have suggested an ecological association between body coloration and wing plasticity strength in the pea aphid, so we tested the hypothesis that the body colour determination locus (tor) associated with wing plasticity variation. We discover that there is no relationship between body colour and wing plasticity in natural populations or in a genetic mapping population. We also localise the tor locus to the third autosome, whereas it was previously thought to be on the first autosome, a finding that will be important for future studies of the locus. We find that the presence of the bacterial symbiont Regiella is associated with higher levels of wing plasticity. Genome-wide association analysis of wing plasticity variation did not reveal an impact of the tor locus, consistent with independence of body colour and wing plasticity. This analysis implicated one possible candidate gene-a Hox gene, abdominal-A-underlying wing plasticity variation, although SNPs do not reach the level of genome-wide significance and therefore will require further study. Our study highlights that plasticity variation is complex, impacted by a bacterial symbiont and genetic variation, but not influenced by body colour.